Ecological niche models as hypothesis generators of functional genetic differentiation and potential local adaptation in a Mediterranean alpine ecosystem

Abstract

Geographically disparate populations within a species’ range may show important differences including variation in ecological, demographic, genetic and phenotypic characteristics. Based on the Center-Periphery Hypothesis, it is often assumed that environmental conditions are optimal in the geographic center of the range and stressful or suboptimal at the periphery, implying ecological marginality is concordant with geographic periphery. But this assumption has been challenged as geographical and ecological gradients are not necessarily concordant. The conservation value of populations inhabiting environmentally marginal areas is still under debate and is closely related with their evolutionary potential. Strong selective pressures caused by stressful conditions may generate novel adaptations in marginal areas, conferring these populations distinct evolutionary potential. But populations inhabiting marginal areas may also show reductions in neutral and adaptive genetic diversity via drift and inbreeding.In this work we explore the potential of ecological niche models (ENMs) to identify environmentally optimal and marginal areas, as well as the principal putative selective pressures likely to act. To do so, we built a carefully parameterized ENM of Silene ciliata, a dominant plant species of Mediterranean alpine habitats. Complementarily, we selected wild populations inhabiting contrasting environmental conditions and carried out common garden experiments to detect genetic differentiation among populations associated with functional traits. With the resulting information, we tested whether environmentally marginal populations defined by the ENM had genetically differentiated phenotypes that are potentially adaptive and, thus, of conservation value.We found genetically based phenotypic differentiation of phenological traits between populations inhabiting areas identified by the ENM as marginal and optimal, as well as between populations with different habitat suitability values. Results supported ENMs as powerful tools for determining environmental marginality and identifying selection pressures, and thus also as hypothesis generators for divergent selection. Furthermore, genetically based phenotypic differentiation found underlines the potential adaptive value of populations inhabiting marginal areas. The approach developed here provides a theoretically justified and practical way to study adaptive processes and provide insights about the conservation value of marginal populations.

Gene flow effects on populations inhabiting marginal areas: Origin matters

“…Environmental variation within the distribution area of S. ciliata in the Sistema Central was previously studied by modelling potential habitat suitability (hereafter, HS) using the MAXENT algorithm (Phillips, Anderson, & Schapire, 2006). Potential HS was based on the occurrence probability of this species in each mountain range (Morente‐Lopez et al., 2020). We defined optimal and marginal environments based on the environmental differentiation summarized by HS and relying on the ecological definition of centrality and marginality (Pironon et al., 2017; Soule, 1973).…”

“…(a) Silene ciliata ecological classification in optimal, intermediate and marginal areas in Guadarrama mountain range (Sistema Central of the Iberian Peninsula). The classification was made by modelling the potential habitat suitability of the territory using the MAXENT algorithm, categorizing habitat suitability values into optimal, intermediate and marginal classes and projecting them in the space (see Appendix ; Morente‐Lopez et al., 2020). (b) Environmental differences between optimal and marginal areas regarding the main environmental variables (minimum annual temperature and snowpack accumulation in thaw months; February, March and April).…”

Ecological niche modeling, niche overlap, and good old Rabinowitz’s rarities applied to the conservation of gymnosperms in a global biodiversity hotspot

“…Therefore, the comparison between different geographic areas within the same species may be of interest to detect areas with divergent evolutionary potential. As ENMs are independent of genetic or phenotypic based adaptive responses, research of potential speciation mechanisms and the development of regional-scale conservation strategies might be of interest (Morente-López et al 2020). From the evolutionary point of view, the observed disjunction between populations might indicate gene flow barriers, affecting between sectors connectivity, that in turn might encourage reproductive isolation through genetic divergence (Blanquart et al 2013).…”

“…ENMs are correlative models unrelated to the biological processes underlying genetic differentiation and adaptation of a species to its environment (Morente-López et al 2020), so they can identify areas with different levels of environmental suitability for a species within its range. In this way, ENMs allow, not only to estimate the distribution of a species and identify putative important environmental variables that shape it (Searcy and Shaffer 2016), but also to postulate hypotheses on divergent selection within a species' range (Blanquart et al 2013).…”